M-CSF signals through the MAPK/ERK pathway via Sp1 to induce VEGF production and induces angiogenesis in vivo

PLoS ONE

Volumn 3, Issue 10, 2008, Pages

  Curry, Jennifer M ^a,b   Eubank, Tim D ^a,c   Roberts, Ryan D ^a,b   Wang, Yijie ^a,c   Pore, Nabendu ^d   Maity, Amit ^d   Marsh, Clay B ^a,b,c  

^a OHIO STATE UNIVERSITY   (United States)

^b THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^c OHIO STATE UNIVERSITY   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLONY STIMULATING FACTOR 1; HYPOXIA INDUCIBLE FACTOR 1; LUCIFERASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PREGNANCY SPECIFIC BETA1 GLYCOPROTEIN; VASCULOTROPIN; VASCULOTROPIN ANTIBODY; TRANSCRIPTION FACTOR SP1; VASCULOTROPIN A;

ANGIOGENESIS; ARTICLE; BINDING SITE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME INHIBITION; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MOLECULAR MECHANICS; MONOCYTE; NUCLEOTIDE SEQUENCE; PHAGOCYTE; PROMOTER REGION; PROTEIN BINDING; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ACTIVE TRANSPORT; ANIMAL; BIOSYNTHESIS; CELL CULTURE; GENETICS; METABOLISM; MOUSE; PHYSIOLOGY;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELLS, CULTURED; HUMANS; MACROPHAGE COLONY-STIMULATING FACTOR; MAP KINASE SIGNALING SYSTEM; MICE; MONOCYTES; NEOVASCULARIZATION, PHYSIOLOGIC; SP1 TRANSCRIPTION FACTOR; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 54449085397     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0003405     Document Type: Article

References (43)

1. Kelley TW, Graham MM, Doseff AI, Pomerantz RW, Lau SM, et al. (1999) Macrophage colony-stimulating factor promotes cell survival through Akt/ protein kinase B. J Biol Chem 274: 26393-26398. doi:10.1074/ jbc.274.37.26393.
2. Hamilton JA, Vairo G, Lingelbach SR (1988) Activation and proliferation signals in murine macrophages: Stimulation of glucose uptake by hemopoietic growth factors and other agents. J Cell Physiol 134: 405-412. doi:10.1002/jcp.1041340311.
3. Junttila I, Bourette RP, Rohrschneider LR, Silvennoinen O (2003) M-CSF induced differentiation of myeloid precursor cells involves activation of PKC-δ and expression of pkare. J Leukoc Biol 73: 281-288. doi:10.1189/jlb.0702359
4. Falkenburg JH, Harrington MA, Walsh WK, Daub R, Broxmeyer HE (1990) Gene-expression and release of macrophage-colony stimulating factor in quiescent and proliferating fibroblasts. effects of serum, fibroblast growth-promoting factors, and IL-1. J Immunol 144: 4657-4662.
5. Misago M, Tsukada J, Ogawa R, Kikuchi M, Hanamura T, et al. (1993) Enhancing effects of IL-2 on M-CSF production by human peripheral blood monocytes. Int J Hematol 58: 43-51.
6. Green M, Harrington MA (2000) A comparison of macrophage colony-stimulating factor (M-CSF) gene expression in primary and immortalized endothelial cells. J Hematother Stem Cell Res 9: 237-246. doi:10.1089/152581600319450.
7. Mancino AT, Klimberg VS, Yamamoto M, Manolagas SC, Abe E, et al. (2001) Breast cancer increases osteoclastogenesis by secreting M-CSF and upregulating RANKL in stromal cells. J Surg Res 100: 18-24. doi:10.1006/ jsre.2001.6204.
8. Wang JM, Griffin JD, Rambaldi A, Chen ZG, Mantovani A (1988) Induction of monocyte migration by recombinant macrophage colony-stimulating factor. J Immunol 141: 575-579.
9. Lu Y, Cai Z, Galson DL, Xiao G, Liu Y, et al. (2006) Monocyte chemotactic protein-1 (MCP-1) acts as a paracrine and autocrine factor for prostate cancer growth and invasion. Prostate 66: 1311-1318. doi:10.1002/pros.20464.
10. Baran CP, Zeigler MM, Tridandapani S, Marsh CB (2004) The role of ROS and RNS in regulating life and death of blood monocytes. Curr Pharm Des 10: 855-866. doi:10.2174/1381612043452866.
11. Varticovski L, Druker B, Morrison D, Cantley L, Roberts T (1989) The colony stimulating factor-1 receptor associates with and activates phosphatidylinositol-3 kinase. Nature 342: 699-702. doi:10.1038/342699a0.
12. Himes SR, Sester DP, Ravasi T, Cronau SL, Sasmono T, et al. (2006) The JNK are important for development and survival of macrophages. J Immunol 176: 2219-2228.
13. Gobert Gosse S, Bourgin C, Liu WQ, Garbay C, Mouchiroud G (2005) M-CSF stimulated differentiation requires persistent MEK activity and MAPK phosphorylation independent of Grb2-sos association and phosphatidylinositol 3-kinase activity. Cell Signal 17: 1352-1362. doi:10.1016/j.cellsig.2005.02.002.
14. Yu Y, Sato JD (1999) MAP kinases, phosphatidylinositol 3-kinase, and p70 S6 kinase mediate the mitogenic response of human endothelial cells to vascular endothelial growth factor. J Cell Physiol 178: 235-246. doi:10.1002/(SICI)1097-4652 (199902)178:2,235::AID-JCP13.3.0.CO;2-S.
15. Besse A, Trimoreau F, Praloran V, Denizot Y (2000) Effect of cytokines and growth factors on the macrophage colony-stimulating factor secretion by human bone marrow stromal cells. Cytokine 12: 522-525. doi:10.1006/ cyto.1999.0580.
16. Richard DE, Berra E, Gothie E, Roux D, Pouyssegur J (1999) p42/p44 mitogenactivated protein kinases phosphorylate hypoxia-inducible factor 1alpha (HIF-1alpha) and enhance the transcriptional activity of HIF-1. J Biol Chem 274: 32631-32637. doi:10.1074/jbc.274.46.32631.
17. Pore N, Liu S, Shu HK, Li B, Haas-Kogan D, et al. (2004) Sp1 is involved in akt-mediated induction of VEGF expression through an HIF-1-independent mechanism. Mol Biol Cell 15: 4841-4853. doi:10.1091/ mbc.E04-05-0374.
18. Milanini J, Vinals F, Pouyssegur J, Pages G (1998) p42/p44 MAP kinase module plays a key role in the transcriptional regulation of the vascular endothelial growth factor gene in fibroblasts. J Biol Chem 273: 18165-18172. doi:10.1074/jbc.273.29.18165.
19. McDermott RS, Deneux L, Mosseri V, Vedrenne J, Clough K, et al. (2002) Circulating macrophage colony stimulating factor as a marker of tumour progression. Eur Cytokine Netw 13: 121-127.
20. Scholl SM, Lidereau R, de la Rochefordiere A, Cohen-Solal Le-Nir C, Mosseri V, et al. (1996) Circulating levels of the macrophage colony stimulating factor CSF-1 in primary and metastatic breast cancer patients. A pilot study. Breast Cancer Res Treat 39: 275-283. doi:10.1007/BF01806155.
21. Sasaki A, Iwashita Y, Shibata K, Matsumoto T, Ohta M, et al. (2006) Prognostic value of preoperative peripheral blood monocyte count in patients with hepatocellular carcinoma. Surgery 139: 755-764. doi:10.1016/j.surg.2005.10.009.
22. Yuan A, Yu CJ, Chen WJ, Lin FY, Kuo SH, et al. (2000) Correlation of total VEGF mRNA and protein expression with histologic type, tumor angiogenesis, patient survival and timing of relapse in non-small-cell lung cancer. Int J Cancer 89: 475-483. doi:10.1002/ 1097-0215(20001120)89:6,475::AID-IJC2>3.0.CO;2-T.
23. Gasparini G (2000) Prognostic value of vascular endothelial growth factor in breast cancer. Oncologist 5: 37-44. doi:10.1634/ theoncologist.5-suppl_1-37.
24. Majer M, Akerley W, Kuwada SK (2007) Oncologists' current opinion on the treatment of colon carcinoma. Anticancer Agents Med Chem 7: 492-503.
25. Gridelli C, Maione P, Rossi A, De Marinis F (2007) The role of bevacizumab in the treatment of non-small cell lung cancer: Current indications and future developments. Oncologist 12: 1183-1193. doi:10.1634/theoncologist.12-10-1183.
26. Eubank TD, Galloway M, Montague CM, Waldman WJ, Marsh CB (2003) MCSF induces vascular endothelial growth factor production and angiogenic activity from human monocytes. J Immunol 171: 2637-2643.
27. Marsh CB, Pomerantz RP, Parker JM, Winnard AV, Mazzaferri Jr EL, et al. (1999) Regulation of monocyte survival in vitro by deposited IgG: Role of macrophage colony-stimulating factor. J Immunol 162: 6217-6225.
28. Eubank TD, Roberts R, Galloway M, Wang Y, Cohn DE, et al. (2004) GM-CSF induces expression of soluble VEGF receptor-1 from human monocytes and inhibits angiogenesis in mice. Immunity 21: 831-842. doi:10.1016/ j.immuni.2004.10.011.
29. Bhatt NY, Kelley TW, Khramtsov VV, Wang Y, Lam GK, et al. (2002) Macrophage-colony-stimulating factor-induced activation of extracellular-regulated kinase involves phosphatidylinositol 3-kinase and reactive oxygen species in human monocytes. J Immunol 169: 6427-6434.
30. Wang Y, Zeigler MM, Lam GK, Hunter MG, Eubank TD, et al. (2007) The role of the NADPH oxidase complex, p38 MAPK, and Akt in regulating human monocyte/macrophage survival. Am J Respir Cell Mol Biol 36: 68-77. doi:10.1165/rcmb.2006-0165OC.
31. Smith JL, Schaffner AE, Hofmeister JK, Hartman M, Wei G, et al. (2000) ets-2 is a target for an akt (Protein kinase B)/jun N-terminal kinase signaling pathway in macrophages of motheaten-viable mutant mice. Mol Cell Biol 20: 8026-8034. doi:10.1128/MCB.20.21.8026-8034.2000.
32. Berra E, Pages G, Pouyssegur J (2000) MAP kinases and hypoxia in the control of VEGF expression. Cancer Metastasis Rev 19: 139-145. doi:10.1023/A1026506011458.
33. Li YM, Zhou BP, Deng J, Pan Y, Hay N, et al. (2005) A hypoxia-independent hypoxia-inducible factor-1 activation pathway induced by phosphatidylinositol-3 kinase/Akt in HER2 overexpressing cells. Cancer Res 65: 3257-3263.
34. Ramos MC, Steinbrenner H, Stuhlmann D, Sies H, Brenneisen P (2004) Induction of MMP-10 and MMP-1 in a squamous cell carcinoma cell line by ultraviolet radiation. Biol Chem 385: 75-86. doi:10.1515/BC.2004.010.
35. Novak EM, Metzger M, Chammas R, da Costa M, Dantas K, et al. (2003) Downregulation of TNF-alpha and VEGF expression by Sp1 decoy oligodeoxynucleotides in mouse melanoma tumor. Gene Ther 10: 1992-1997. doi:10.1038/sj.gt.3302111.
36. Varney ML, Olsen KJ, Mosley RL, Singh RK (2005) Paracrine regulation of vascular endothelial growth factor-a expression during macrophage-melanoma cell interaction: Role of monocyte chemotactic protein-1 and macrophage colony-stimulating factor. J Interferon Cytokine Res 25: 674-683. doi:10.1089/jir.2005.25.674.
37. Okazaki T, Ebihara S, Asada M, Yamanda S, Saijo Y, et al. (2007) Macrophage colony-stimulating factor improves cardiac function after ischemic injury by inducing vascular endothelial growth factor production and survival of cardiomyocytes. Am J Pathol 171: 1093-1103. doi:10.2353/ajpath.2007.061191.
38. Pages G, Berra E, Milanini J, Levy AP, Pouyssegur J (2000) Stress-activated protein kinases (JNK and p38/HOG) are essential for vascular endothelial growth factor mRNA stability. J Biol Chem 275: 26484-26491. doi:10.1074/jbc.M002104200.
39. Milanini-Mongiat J, Pouyssegur J, Pages G (2002) Identification of two Sp1 phosphorylation sites for p42/p44 mitogen-activated protein kinases: Their implication in vascular endothelial growth factor gene transcription. J Biol Chem 277: 20631-20639. doi:10.1074/jbc.M201753200.
40. Dery MA, Michaud MD, Richard DE (2005) Hypoxia-inducible factor 1: Regulation by hypoxic and non-hypoxic activators. Int J Biochem Cell Biol 37: 535-540. doi:10.1016/j.biocel.2004.08.012.
41. Leonard EJ, Yoshimura T (1990) Human monocyte chemoattractant protein-1 (MCP-1). Immunol Today 11: 97-101. doi:10.1016/0167-5699(90)90035-8.
42. Varney ML, Olsen KJ, Mosley RL, Bucana CD, Talmadge JE, et al. (2002) Monocyte/macrophage recruitment, activation and differentiation modulate interleukin-8 production: A paracrine role of tumor-associated macrophages in tumor angiogenesis. In Vivo 16: 471-477.
43. Tojo N, Asakura E, Koyama M, Tanabe T, Nakamura N (1999) Effects of macrophage colony-stimulating factor (M-CSF) on protease production from monocyte, macrophage and foam cell in vitro: A possible mechanism for anti-atherosclerotic effect of M-CSF. Biochim Biophys Acta 1452: 275-284. doi:10.1016/S0167-4889(99)00127-5.